Kalinda et al. Infectious Diseases of Poverty (2017) 6:57 DOI 10.1186/s40249-017-0260-z

RESEARCH ARTICLE Open Access Effect of temperature on the globosus — system Chester Kalinda1*, Moses J. Chimbari1 and Samson Mukaratirwa2

Abstract Background: Given that increase in temperature may alter host-parasite relationships, the anticipated rise in temperature due to global warming might change transmission patterns of certain diseases. However, the extent to which this will happen is not well understood. Methods: Using a host-parasite system involving Bulinus globosus and Schistosoma haematobium, we assessed the effect of temperature on snail fecundity, growth, survival and parasite development under laboratory conditions. Results: Our results show that temperature may have a non-linear effect on snail fecundity and snail growth. Snails maintained at 15.5 °C and 36.0 °C did not produce egg masses while those maintained at 25.8 °C laid 344 and 105 more egg masses than snails at 31.0 °C and 21.2 °C, respectively. Attainment of patency led to a reduction in egg mass production among the snails. However, the reduction in fecundity for snails maintained at 21.2 °C occurred before snails started shedding cercariae. Parasite development was accelerated at high temperatures with snails maintained at 31.0 °C reaching patency after three weeks. Furthermore, snail growth rate was highest at 25.8 °C while it was inhibited at 15.5 °C and reduced at 31.0 °C. Increase in temperature increased snail mortality rates. Snails maintained at 36.0 °C had the shortest survival time while those maintained at 15.5 °C had the longest survival time. Conclusions: We concluded that temperature influences fecunxdity, growth, survival and parasite development in the snail and thus dictates the time it takes the parasite to complete the life cycle. This has implications on transmission of schistosomiasis in the context of global warming. Keywords: Bulinus globosus, Cercariae, Development rate, Fecundity, Schistosomiasis, Schistosoma haematobium, Temperature

Multilingual abstracts temperature [3]. Temperature influences the physiology, Please see Additional file 1 for translations of the ecology, susceptibility of snails to infection and parasite abstract into the five official working languages of pathogenicity [4–7]. Earlier studies [8–10] observed that the United Nations. B. globosus, the intermediate host snail of S. haemato- bium, had high thermal tolerance and adapted in areas with fluctuating temperature [11, 12]. This snail has also Background been observed to have marked increase in survival time at Schistosomiasis is a parasitic disease caused by blood fluke temperatures as high as 34.0 °C [6] while its optimal trematodes of the genus Schistosoma [1]. Schistosoma temperature for fecundity and growth has been shown to haematobium and Schistosoma mansoni are the two be 25.0 °C [11]. Furthermore, this temperature coincides major species affecting people in southern Africa [1, 2]. with the optimal temperature range (22 – 27 °C) for Different stages of the disease cycle are affected by disease transmission [13]. This suggests that the antici- pated rise in temperature due to climate change may have * Correspondence: [email protected] 1School of Nursing and Public Health, College of Health Sciences, Howard serious implications on snail population size and schisto- College Campus, University of KwaZulu-Natal, Durban, South Africa somiasis spread patterns. Full list of author information is available at the end of the article

© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kalinda et al. Infectious Diseases of Poverty (2017) 6:57 Page 2 of 7

The effect of temperature on the growth and reproduction (15.0, 20.0, 25.0, 30.0 and 35.0 °C). Three aquaria were of snails may influence the development rates of parasites assigned to each experimental temperature and each and hosts [14]. Growing evidence suggests that under future aquaria contained three 2 L containers holding nine global warming scenarios, host population dynamics may snails. The total number of snails per temperature treat- play vital roles in determining disease spread patterns and ment was 81. Each snail was individually exposed to three parasite output load [15]. Temperature promotes the devel- miracidia following methods described by Mukaratirwa et opment of hosts and parasites while reducing their survival al. [22]. The snails were fed ad libitum on blanched let- [16] suggesting that its net effect on host development and tuce and supplemented with Tetramin tropical fish food population size may be important in determining disease (Marltons Pet care products). Before the start of the spread and parasitism levels. Contrasting observations on experiments, snails were allowed to acclimatize to their re- the potential effects of temperature rise on snails have been spective experimental temperatures for one week. During made. Pedersen et al. [17] and Martens et al. [18] suggested the course of the experiments, the containers within the a possible reduction in habitat suitability and disease trans- aquaria were rotated weekly to avoid positional effects mission while Zhou et al. [19] and McCreesh et al. [20] [23]. The snails were kept in an experimental room with a suggested that a rise in temperature may lead to an increase photoperiod of 12:12 h light–dark cycle. in suitable habitats and schistosomiasis prevalence. Furthermore, Nelson et al. [21] suggested that adap- Maintenance of constant water temperature tion of snails to higher temperatures may affect their Each aquarium was filled with tap water to provide a susceptibility to infection. water bath for maintaining specific water temperature In view of these conflicting potential outcomes of climate regulated by a 250 W aquarium heater (JERO 2010 Life- change on schistosomiasis risks, understanding the possible Tech) and gas tubes were placed in each aquarium for effects of temperature on snails through mechanistic ap- circulating the water to maintain uniform temperature. proaches may show the broad potential impacts of climate The 2 L containers placed in the aquaria were filled with change on the transmission of schistosomiasis. This will filtered pond water which was changed once a week. A also assist in understanding the potential influence of small polystyrene plate was placed in each 2 L container temperature changes on patterns of snail growth, fecundity, for collecting egg masses. For the pre-determined tem- survival and parasite development. Using B. globosus,we peratures of 15.0, 20.0, 25.0, 30.0 and 35.0 °C, the mean experimentally assessed the effect of S. haematobium infec- (±SE) water temperature that was achieved was: 15.5 ± tion and temperature on the fecundity, survival and growth 0.39, 21.2 ± 0.83, 25.8 ± 0.66, 31.0 ± 0.44 and 36.0 ± of the intermediate host snails and production of cercariae. 0.35 °C. The study developed a mechanistic host-parasite model for understanding the potential impacts of future temperature Measurement of fecundity, survival and growth rise on the snail-trematode system. parameters To evaluate the fecundity of B. globosus, we counted the Methods number of egg masses deposited on the polystyrene Breeding of experimental plates and walls of the containers over a nine-week period. Sexually mature B. globosus snails were collected from The egg masses were collected, counted and removed uMkhanyakude and Verulam in KwaZulu-Natal Province, from the polystyrene plates and walls of the containers South Africa and kept in 2 litre (L) containers filled with every two days. These were then aggregated to compose a filtered pond water. A small polystyrene plate substrate week’s collection. was put in the 2 L containers to provide a surface for Snail mortality was recorded daily across the different snails to lay eggs on. Egg masses deposited on the poly- temperature treatments. Snails were marked as dead if styrene plates and on the walls of the containers were they did not respond to mechanical stimuli while those removed as soon as they were noticed and transferred to that showed signs of movements were returned to their new containers for hatching at room temperature. The experimental temperature treatments [24]. hatchlings were pooled to constitute the first generation Snail shell heights were measured at the beginning of (F-1) which was the study population. First generation the experiment and thereafter at two weekly intervals for snails with an average shell height of 3 – 4mmwereused determination of growth. Fifteen snails from each aquarium for the experiments. (45 snails from each temperature treatment) were randomly selected and their shell heights were measured to the Study animals and experimental set up nearest 0.1 mm using vernier callipers (Mitutoyo Four hundred and five laboratory bred F-1 B. globosus Corp) following methods described by Doums et al. juveniles were randomly selected and allocated to fifteen [25]. The measurement of snail shell height was done 20 L aquaria maintained at five constant temperatures over a period of 10 weeks. Kalinda et al. Infectious Diseases of Poverty (2017) 6:57 Page 3 of 7

Cercaria counts To determine how temperature influenced the onset From three weeks post infection, all snails were indi- of cercariae shedding, a proportional hazard test was vidually exposed to artificial light in shedding tubes to used. For this analysis, snails exposed to miracidia induce cercariae shedding. Snails that shed cercariae but which did not shed cercariae were labelled as were transferred to new 2 L containers and returned to censored [23]. their respective aquarium. The water in the shedding We estimated the total number of cercariae shed at each j tubes was transferred to corning tubes and 70% ethanol experimental temperature as: Tc = ∑i =1 Pi * Ci * Ai [28] was added to preserve the cercariae for later counting. where Tc is the total number of cercariae released, Pi is the Cercariae shedding was continued until the 77th day post proportion of snails shedding cercariae on a particular infection. Counting of cercariae was done in accordance shedding time point i, Ci is the number of cercariae ob- with the methods described by Paull et al. [26] and tained from the shedding jars of snails shedding cercariae McClelland [27]. and Ai is the number of snails alive at that temperature The experiments were terminated at day 80 post infec- treatment at time i. tion. This was done to ensure that the longest pre-patent All analyses were conducted using Stata (StataCorp, period was catered for and data related to growth and 2013) and Graphpad Prism 5 for Windows (Graphpad fecundity was collected. Snails that did not shed cercariae software, San Diego, California, USA). from the different experimental temperature treatments were dissected and examined for presence or absence of Results sporocysts using a dissecting microscope. Snail fecundity Bulinus globosus snails maintained at average tempera- Data analysis tures of 15.5 and 36.0 °C did not lay egg masses while To determine the influence of temperature on host fe- those maintained at 21.2, 25.8 and 31.0 °C did. Time (P< cundity, an analysis of variance (ANOVA) with Repeated 0.001) and temperature (P<0.001) affected the number of Measures (RM) was used. Egg mass counts were square egg masses that were deposited. Egg mass production root transformed to improve homogeneity of variance gradually increased during the pre-patent period for all before being used in the RM ANOVA. Survival analysis treatment except in the case of 21.2 °C where the decline was used to determine the influence of temperature on occured one week before patency (Fig. 1). Bulinus globosus survival time of snails. The survival times were com- snails maintained at 21.2 °C produced 1 254 egg masses pared between the different temperature groups using while those at 25.8 and 31.0 °C produced 1 359 and 1 015 the Log Rank (Mantel-cox) tests. egg masses, respectively.

Fig. 1 Weekly number of egg masses produced by Bulinus globosus maintained at (a) 21.2, (b) 25.8 and (c) 31.0 °C Kalinda et al. Infectious Diseases of Poverty (2017) 6:57 Page 4 of 7

Snail survival Table 1 Comparisons in the survival time of Bulinus globosus As temperature increased, the median survival time snails maintained at different temperature levels reduced (P = 0.001). The snails maintained at 36.0 °C Temperature (°C) groups Chi-square Hazard ratio 95% CI of ratio had the lowest survival rate of 8.64% while those main- 15.5 vs 21.2 6.470 0.224* 0.071 – 0.709 tained at 15.5 °C had a survival rate of 87.6% (Fig. 2). 15.5 vs 25.8 5.450 0.238* 0.072 – 0.795 The survival time of snails maintained at 21.2 and 25.8 °C 15.5 vs 31.0 42.400 0.063*** 0.027 – 0.144 was not significantly different (Log Rank (Mantel-cox) test: – P = 0.675). However, significant differences (P<0.001) in 21.2 vs 25.8 0.176 0.827 0.339 2.014 the survival time were observed between snails maintained 21.2 vs 31.0 16.050 0.223*** 0.107 – 0.465 at 25.8 and 31.0 °C. Those maintained at 15.5 °C had longer 25.8 vs 31.0 11.920 5.182*** 2.459 – 10.92 survival time and least hazard ratios as compared to snails Significance codes: *0.05, ***0.0001 maintained at other temperatures (Table 1). intermediate host snails. Although egg mass production Cercariae counts observed at the three temperature levels seemed to have Increasing temperature had a positive effect on the length been accelerated during the early stages of infection, of the pre-patent period (P<0.01). Snails maintained at attainment of patency led to a reduction in the egg mass 31.0 °C reached patency after three weeks post infection output. This may be due to the rise in the competition for while those at 21.2 °C reached patency after six weeks. resources by the developing parasites within the host Temperature and time had a significant (Temperature: P snails. According to Sorensen and Minchella [29], intra- = 0.0076, Time: P<0.001) influence on the number of molluscan parasite development leads to changes in the cercariae shed from snails. Over time, there was an host energy allocation patterns. Parasites have also been ’ increase in the number of cercariae shed, followed by a re- observed to deplete the hosts energy used for gamete pro- duction. The estimated mean (± SE) number of cercariae duction and egg formation which leads to a reduction in shed at 31.0, 25.8 and 21.2 °C was 829 ± 224.4, 2 409 ± the reproduction capacity of the host [30]. Our results 488.9 and 1 738 ± 409.9 respectively. indicate that while temperature rise was observed to accel- erate gametogenesis [31] leading to increased egg mass output, parasitic infection may result in host fecundity Snail growth reduction which may have implications on the host It was observed that increasing temperature influenced population size. This is in agreement with the observa- snail growth rate significantly (P<0.001). Snails main- tions made by Fryer et al. [32], Minchella and Loverde tained at 15.5 °C had inhibited growth while those at [33], Muñoz-Antoli et al. [34], Jourdane [35] and Paull 31.0 °C had reduced growth (Fig. 3). The results also and Johnson [23]. Temperature may lead to an increase in show that the growth rate of B. globosus was higher during snail fecundity in some areas with tolerable temperature the pre-patent period compared to the patent period levels and a reduction in areas with low and very high (Fig. 3). temperatures. Nevertheless, its net effect may have conse- quences on the parasite load in the natural environment. Discussion Snail survival was greatly affected by temperature with The reduction in egg mass laying during the patent period snails maintained at higher temperature having reduced shows that trematode infection affects the fecundity of the survival time. All the snails that were maintained at 36.0 °C did not survive beyond the fourth week of the experiment. These findings are similar to those of Woolhouse and Chandiwana [36] who observed that snail mortality increased linearly with temperature above 24.0 °C. The increase in snail mortality may sug- gest that extreme high temperatures may be unsuit- able for the development of snails. With temperature projected to increase due to climate change [37, 38], areas with extreme high temperatures may record reduced snail population sizes [39] which might lead to a reduction in the disease prevalance. Nevertheless, areas with temperatures around 31.0 °C may experience possible disease transmission because of snail availability. Snail Fig. 2 Mortality rates of Bulinus globosus maintained at 15.5, 21.2, longevity at this temperature was reduced. Nonetheless, 25.8, 31.0 and 36.0 °C the snails remained fecund, suggesting that juvenile snails Kalinda et al. Infectious Diseases of Poverty (2017) 6:57 Page 5 of 7

Fig. 3 Weekly growth rate of Bulinus globosus maintained at (a) 15.5, (b) 21.2, (c) 25.8 and (d) 31.0 °C may be introduced to the environment. Bulinus globosus as temperature increases while low temperatures inhibit snails have been observed to inhabit moist muddy soils or parasite development [23]. An earlier study by Pfluger et hide under floating aquatic plants [12, 40]. Prolonged hot al. [46] observed that B. truncatus snails exposed to summer temperatures may lead to drying out of moist 15.3 °C did not shed cercariae. This is supported by our areas and aquatic vegetation that provide shelter to snails. findings which also showed that at 15.5 °C, B. globosus This may also lead to a possible reduction in the snail did not develop infection. This means that at this population size [41]. All this suggests that endemic temperature, disease transmission may also be reduced. areas with high temperatures may have reduced snail The optimal temperature range for the transmission of population size which can also impact on the disease schistosomiasis is 22 – 27 °C [13]. On the other hand, transmission. the fact that sufficiently high snail survival rate was It was also observed that mortality of snails at 25.8 °C observed at 15.5 °C suggests that high snail proliferation was high but maximal egg mass output was still achieved may occur when temperature is increased. This may lead at this temperature. This increased egg mass output may to a possible increase in the prevalence of schistosomia- be attributed to the ability of B. globosus to increase its sis in certain areas [45]. This may be the case in some egg mass production as temperature approaches or endemic areas which experience low temperatures slightly exceeds 25.0 °C [11, 12]. According to Shiff [13], during the winter season. Paull and Johnson [23] observed B. globosus maintains its optimal net reproductive rate that cercariae can develop in snails previously maintained (R0) at 25.0 °C. Our results comfirm findings from other at low temperature if the maintenance temperature rises studies [11, 13, 42] that suggest that temperatures above the minimum cercariae development temperature around and slightly above 25.0 °C may lead to increased threshold. This suggests that snails surviving the cold egg mass output. Coupled with increased growth rate of winter seasons in endemic areas may serve as the source snails maintained at 25.8 °C (Fig. 3), this temperature of early infection as temperatures become favourable for may lead to early development of parasites, thus increasing parasite development. the disease risks in areas experiencing this temperature. Our study also suggests that establishment of S. Despite this, the parasites’ effect on the ovotestis of hosts haematobium within the host snails may lead to notable [1, 43] which was observed to lead to castration of snails alteration in the hosts’ life history traits. Infected snails [23, 44] may offset the positive effect of temperature on have been observed to experience significant loss of snail fecundity. resources for reproduction [30, 43]. Increased growth of According to Martens et al. [18] and Knight et al. [45], infected snails commonly known as gigantism has been temperature influences the infection of snails. Further- reported [23, 29, 34]. Although gigantism has been asso- more, parasite development within the snails increases ciated with trematode infection, variable observations Kalinda et al. Infectious Diseases of Poverty (2017) 6:57 Page 6 of 7

have been made on the effects of parasites on snail Acknowledgements growth. According to Chu et al. [47], the growth rate of The study was done as part of the PhD work for the first author. Many thanks are due to Prof Benn Sartorius for his tremendous input and infected snails was unaffected by trematode infection, reviewing the paper. We also would like to thank the two anonymous while Sorensen and Minchella [48] observed that infec- reviewers who helped improve the quality of the paper. tion led to a reduction in the growth of snails. Our study observed that infection led to an increase in the growth Funding The study received financial support from University of KwaZulu-Natal College of snails and this corroborates the findings of Muñoz- of Health Sciences through the student scholarship programme, and from Antoli et al. [34] and Sturrock [49]. The increase in the United Nations International Children's Fund/United Nations Development sizeofinfectedsnailsmayprobablybeduetotheamount Programme/World Bank/World Health Organization Special Programme for Re- search and Training in Tropical Diseases, and from the Canadian International of resources and energy redirected towards somatic growth Development Research Centre through their support towards a Malaria [50]. On the other hand, the inhibition of snail growth rate and Bilharzia in Southern Africa project. at 15.5 °C and its subsequent reduction at 31.0 °C may sug- gest possible effects of extreme low and high temperatures Availability of data and materials The data that has been used will be archived and stored at the project centre on snail development and eventual parasite production. of the Malaria and Bilharzia in Southern Africa (MABISA) project, University of Furthermore, Nelson et al. [21] suggest that acclimatization KwaZulu-Natal. Data can be requested by following the guidelines laid out in of snails to higher temperature may occur. This may thus the Data Access Policy of the University of KwaZulu-Natal. change both the population dynamics and infection rates of Authors’ contributions snails at higher temperatures. The current study observed KC, SM and MJC conceptualised the study. KC developed the methodology, that snail growth rate was optimum at 25.8 °C and this is collected the data, performed the analysis, and wrote the manuscript. MJC similar to the findings of Harrison and Shiff [11]. An and SM read and edited the manuscript. All the authors approved the final increase in snail growth and fecundity around this version and agree to be accountable for any aspects of the work. temperature range may have implications on schisto- Competing interests somiasis prevalence. The authors declare that they have no competing interests.

Consent for publication Conclusion Not applicable. The results suggest that such a mechanistic study model can provide useful information for developing mathem- Ethics approval and consent to participate atical models that assess and predict the likely changes All experimental protocols and procedures of this study were reviewed and in the snail populations as a result of temperature approved by the Animals Ethics Committee of the University of KwaZulu-Natal (UKZN) (Ref: AREC 027/016D) in accordance with the South African national change. Although our study has shown some of the guidelines on care, handling and use for biomedical research. direct effects of temperature rise on snail growth rate and parasite production, there is furthermore a need to Author details 1School of Nursing and Public Health, College of Health Sciences, Howard identify the likely secondary alterations in parasite trans- College Campus, University of KwaZulu-Natal, Durban, South Africa. 2School mission that may be the outcome of temperature driven of Life Sciences, College of Agriculture, Engineering and Science, Westville changes in the snail-trematode system. The study has Campus, University of KwaZulu-Natal, Durban, South Africa. also shown that B. globosus has a different threshold Received: 3 August 2016 Accepted: 15 February 2017 temperature for reproduction, survival and parasite de- velopment and this will have implications on the spread of schistosomiasis. These findings may also be useful in References 1. Appleton C, Madsen H. Human schistosomiasis in wetlands in southern informing schistosomiasis control programmes by identi- Africa. Wetl Ecol Manag. 2012;20(3):253–69. fying new areas that may be targeted for control initiatives 2. De Kock K, Wolmarans C. Distribution and habitats of the Bulinus africanus on the basis of predicted temperature rises. species group, snail intermediate hosts of Schistosoma haematobium and S. mattheei in South Africa. Water SA. 2005;31(1):117–25. 3. O’keeffe J. Population biology of the Bulinus globosus on Additional file the Kenya coast. I. Population fluctuations in relation to climate. J Appl Ecol. 1985;22(1):73–84. 4. De Kock K, Van Eeden J. Effect of programmed circadian temperature Additional file 1: Multilingual abstracts in the five official working fluctuations on population dynamics of Biomphalaria pfeifferi (Krauss). S Afr languages of the United Nations. (PDF 820 kb) J Zool. 1986;21(1):28–32. 5. Appleton C. Review of literature on abiotic factors influencing the distribution and life cycles of bilharziasis intermediate host snails. Abbreviations Malacology Review. 1978;11:1–25. Ai: Number of snails alive at that temperature treatment at time i; ANOVA: Analysis 6. Joubert PH, Pretorius SJ, DeKock KN, Vaneeden JA. Survival of Bulinus- of Variance; Ci: Number of cercariae obtained from the shedding jars of snails africanus (Krauss), Bulinus-globosus (Morelet) and Biomphalaria-pfeifferi shedding cercariae; GLM: Generalised Linear Model; L: Litre; Pi: Proportion of snails (Krauss) at constant high-temperatures. S Afr J Zool. 1986;21(1):85–8. shedding cercariae on a particular shedding time point I;RM:Repeated 7. Hakalahti T, Karvonen A, Valtonen ET. Climate warming and disease risks in Measures; Ro: Reproductive number; SE: Standard Error; Tc: Total number temperate regions–Argulus coregoni and Diplostomum spathaceum as case of cercariae; W: Watt studies. J Helminthol. 2006;80(02):93–8. Kalinda et al. Infectious Diseases of Poverty (2017) 6:57 Page 7 of 7

8. Pitchford R, Visser P. The use of behaviour patterns of larval schistosomes in 32. Fryer SE, Oswald RC, Probert AJ, Runham NW. The effect of Schistosoma assessing the bilharzia potential of non-endemic areas. S Afr Med J. haematobium infection on the growth and fecundity of three sympatric 1969;43(32):983–95. species of bulinid snails. J Parasitol. 1990;76(4):557–63. 9. Shiff C, Husting E. An application of the concept of intrinsic rate of 33. Minchella DJ, Loverde PT. A cost of increased early reproductive effort in natural increase to studies on the ecology of freshwater snails of the the snail Biomphalaria glabrata. Am Nat. 1981;118(6):876–81. genera Biomphalaria and Bulinus (Physopsis) in southern Africa. Proc 34. Muñoz-Antoli C, Marín A, Toledo R, Esteban J-G. Effect of Echinostoma friedi Trans Rhodesian Sci Assoc. 1966;51:1–8. (Trematoda: Echinostomatidae) experimental infection on longevity, growth 10. Gordon R, Davey T, Peaston H. The transmission of human bilharziasis in and fecundity of juvenile Radix peregra (: Lymnaeidae) and Sierra Leone, with an account of the life cycle of the schistosomes concerned, Biomphalaria glabrata (Gastropoda: ) snails. Parasitol Res. S. mansoni and S. haematobium. Ann Trop Med Parasitol. 1934;28:323–418. 2007;101(6):1663–70. 11. Harrison A, Shiff C. Factors influencing the distribution of some species of 35. Jourdane J. Effects of hyperinfestations by Echinostoma togoensis Jourdane aquatic snails. S Afr J Sci. 1966;62(25):3–258. and Kulo, 1981 on growth and survival of Biomphalaria pfeifferi snails. Ann 12. Marti H. Field observations on the population dynamics Bulinus globosus, Parasitol Hum Comp. 1982;58(2):103–8. the intermediate host of Schistosoma haematobium in the Ifakara area, 36. Woolhouse M, Chandiwana S. Population dynamics model for Bulinus Tanzania. J Parasitol. 1986;72(1):119–24. globosus, intermediate host for Schistosoma haematobium, in river habitats. 13. Shiff C. Studies on Bulinus (Physopsis) globosus in Rhodesia. I. The influence Acta Trop. 1990;47(3):151–60. of temperature on the intrinsic rate of natural increase. Ann Trop Med 37. Hughes L. Biological consequences of global warming: is the signal already Parasitol. 1964;58:94–105. apparent? Trends Ecol Evol. 2000;15(2):56–61. 14. Stenseth NC, Mysterud A. Climate, changing phenology, and other life 38. Yang G-J, Utzinger J, Sun L-P, Hong Q-B, Vounatsou P, Tanner M, Zhou X-N. history traits: nonlinearity and match–mismatch to the environment. Proc Effect of temperature on the development of Schistosoma japonicum within Natl Acad Sci. 2002;99(21):13379–81. Oncomelania hupensis, and hibernation of O. hupensis. Parasitol Res. 15. Poulin R. Global warming and temperature-mediated increases in cercarial 2007;100(4):695–700. emergence in trematode parasites. Parasitology. 2006;132(01):143–51. 39. McCreesh N, Booth M. The effect of increasing water temperatures on 16. Seppälä O, Jokela J. Immune defence under extreme ambient temperature. Schistosoma mansoni transmission and Biomphalaria pfeifferi population Biol Lett. 2011;7(1):119–22. dynamics: an agent-based modelling study. PLoS One. 2014;9(7):101462. 17. Pedersen UB, Stendel M, Midzi N, Mduluza T, Soko W, Stensgaard A-S, 40. Woolhouse M, Chandiwana S. Spatial and temporal heterogeneity in the Vennervald BJ, Mukaratirwa S, Kristensen TK. Modelling climate change population dynamics of Bulinus globosus and Biomphalaria pfeifferi and in impact on the spatial distribution of fresh water snails hosting trematodes in the epidemiology of their infection with schistosomes. Parasitology. – Zimbabwe. Parasit Vectors. 2014;7(1):1. 1989;98(01):21 34. 18. Martens W, Jetten TH, Focks DA. Sensitivity of malaria, schistosomiasis and 41. Bavia ME, Hale LF, Malone JB, Braud DH, Shane SM. Geographic information dengue to global warming. Clim Chang. 1997;35(2):145–56. systems and the environmental risk of schistosomiasis in Bahia, Brazil. – 19. Zhou XN, Yang GJ, Sun LP, Hong QB, Yang K, Wang RB, Hua ZH. Potential AmJTrop Med Hyg. 1999;60(4):566 72. impact of global warming on the transmission of schistosomiasis. Chinese 42. Shiff CJ, Garnett B. The influence of temperature on the intrinsic rate of – J Epidemiol. 2002;23:83–6. natural increase of the freshwater snail B. pfeifferi. Arch Hydrobiol. 1967;62:429 38. 20. McCreesh N, Nikulin G, Booth M. Predicting the effects of climate change 43. Probst S, Kube J. Histopathological effects of larval trematode infections in on Schistosoma mansoni transmission in eastern Africa. Parasit Vectors. mudsnails and their impact on host growth: what causes gigantism in 2015;8(1):1–9. Hydrobia ventrosa (Gastropoda: Prosobranchia)? J Exp Mar Biol Ecol. – 21. Nelson MK, Cruz BC, Buena KL, Nguyen H, Sullivan JT. Effects of abnormal 1999;238(1):49 68. temperature and starvation on the internal defense system of the schistosome- 44. Lafferty KD. Effects of parasitic castration on growth, reproduction and transmitting snail Biomphalaria glabrata. J Invertebr Pathol. 2016;138:18–23. population dynamics of the marine snail Cerithidea californica. Mar Ecol - 22. Mukaratirwa S, Kristensen TK, Siegismund HR, Chandawana SK. Genetic and Prog Ser. 1993;96:229. morphological variation of populations belonging to the / 45. Knight M, Elhelu O, Smith M, Haugen B, Miller A, Raghavan N, Wellman C, tropicus complex (Gastropoda; Planorbidae) in south western Zimbabwe. Cousin C, Dixon F, Mann V, Rinaldi G, Ittiprasert W, Brindley PJ. Susceptibility J Molluscan Stud. 1998;64(4):435–46. of snails to infection with schistosomes is influenced by temperature and expression of heat shock proteins. Epidemiol (Sunnyvale, Calif). 2015;5(2):189. 23. Paull SH, Johnson PTJ. High temperature enhances host pathology in a doi:10.4172/2161–1165.1000189. snail–trematode system: possible consequences of climate change for the 46. Pfluger W, Roushdy M, El-Emam M. Prepatency of Schistosoma haematobium emergence of disease. Freshw Biol. 2011;56(4):767–78. in snails at different constant temperatures. J Egypt Soc Parasitol. 24. Joubert P, Pretorius S, De Kock K, Van Eeden J. The effect of constant 1983;13(2):513–9. low temperatures on the survival of Bulinus africanus(Krauss), Bulinus 47. Chu K, Massoud J, Sabbaghian H. Host–parasite relationship of Bulinus truncatus globosus(Morelet) and Biomphalaria pfeifferi(Krauss). S Afr J Zool. and Schistosoma haematobium in Iran: 3. Effect of water temperature on the 1984;19(4):314–6. ability of miracidia to infect snails. Bull World Health Organ. 1966;34(1):131. 25. Doums C, Perdieu M-A, Jarne P. Resource allocation and stressful conditions 48. Sorensen R, Minchella D. Snail–trematode life history interactions: past in the aphallic snail Bulinus truncatus. Ecology. 1998;79(2):720–33. trends and future directions. Parasitology. 2001;123:S3–S18. 26. Paull SH, Raffel TR, LaFonte BE, Johnson PTJ: How temperature shifts affect 49. Sturrock B. The effect of infection with Schistosoma haematobium on the parasite production: testing the roles of thermal stress and acclimation. growth and reproduction rates of Bulinus (Physopsis) nasutus productus. Ann Functional Ecology. 2015:1–10. doi:10.1111/1365-2435.12401. Trop Med Parasitol. 1967;61(3):321. 27. McClelland W. The production of cercariae by Schistosoma mansoni and S. 50. Sousa WP. Host life history and the effect of parasitic castration on growth: haematobium and methods for estimating the numbers of cercariae in a field study of Cerithidea californica haldeman (Gastropoda: Prosobranchia) suspension. Bull World Health Organ. 1965;33(2):270. and its trematode parasites. J Exp Mar Biol Ecol. 1983;73(3):273–96. 28. Paull SH, Johnson PT. Experimental warming drives a seasonal shift in the timing of host‐parasite dynamics with consequences for disease risk. Ecol Lett. 2014;17(4):445–53. 29. Sorensen RE, Minchella DJ. Parasiteinfluencesonhostlifehistory: Echinostoma revolutum parasitism of Lymnaea elodes snails. Oecologia. 1998;115(1–2):188–95. 30. Gerard C, Theron A. Age/size-and time-specific effects of Schistosoma mansoni on energy allocation patterns of its snail host Biomphalaria glabrata. Oecologia. 1997;112(4):447–52. 31. Brackenbury T, Appleton C. Effect of controlled temperatures on gametogenesis in the gastropods Physa acuta (Physidae) and Bulinus tropicus (Planorbidae). J Molluscan Stud. 1991;57(4):461–9.